Family matters: skin microbiome reflects the social group and spatial proximity in wild zebra finches

Abstract

Background So far, large numbers of studies investigating the microbiome have focused on gut microbiota and less have addressed the microbiome of the skin. Especially in avian taxa our understanding of the ecology and function of these bacteria remains incomplete. The involvement of skin bacteria in intra-specific communication has recently received attention, and has highlighted the need to understand what information is potentially being encoded in bacterial communities. Using next generation sequencing techniques, we characterised the skin microbiome of wild zebra finches, aiming to understand the impact of sex, age and group composition on skin bacteria communities. For this purpose, we sampled skin swabs from both sexes and two age classes (adults and nestlings) of 12 different zebra finch families and analysed the bacterial communities. Results Using 16S rRNA sequencing we found no effect of age, sex and family on bacterial diversity (alpha diversity). However, when comparing the composition (beta diversity), we found that animals of social groups (families) harbour highly similar bacterial communities on their skin with respect to community composition. Within families, closely related individuals shared significantly more bacterial taxa than non-related animals. In addition, we found that age (adults vs. nestlings) affected bacterial composition. Finally, we found that spatial proximity of nest sites, and therefore individuals, correlated with the skin microbiota similarity. Conclusions Birds harbour very diverse and complex bacterial assemblages on their skin. These bacterial communities are distinguishable and characteristic for intraspecific social groups. Our findings are indicative for a family-specific skin microbiome in wild zebra finches. Genetics and the (social) environment seem to be the influential factors shaping the complex bacterial communities. Bacterial communities associated with the skin have a potential to emit volatiles and therefore these communities may play a role in intraspecific social communication, e.g. via signalling social group membership.

Cloaca‐ and feather‐associated bacteria communities in common waxbills Estrilda astrild

“…For instance, Pseudomonas largely dominated cloaca microbiota with about 60% of the total number of reads, whereas in feathers the relative abundances of bacteria taxa were more equitable, with the most abundant genus ( Sphingomonas ) representing only about 10% of the total number of the reads. Similarly to our results, significant differences of microbiota between body sites were reported for other passerines (cloacal, skin and feathers microbiotas; van Veelen et al 2017, Engel et al 2018, 2020).…”

Host genotype and microbiome associations in co‐occurring clonal and non‐clonal kelp, Ecklonia radiata

“…IBD, Imhann et al, 2018). Another example in birds demonstrates that members of the same family have a more similar skin microbiome in contrast to other families of the same species (Engel et al, 2020). It is important to note that compositional and structural taxonomical differences in microbial communities between individuals may not translate to functional shifts as predicted in the present study.…”

“…Morphological variation between individuals is, to some extent, influenced by the host genotype, but other phenotypic traits that often have a strong genetic component, such as the release of waste compounds, secondary metabolites or the host's immune response, may have a stronger effect on the microbiome (Coyte et al, 2015; Griffiths et al, 2019). Indeed, microbiomes regulated by these traits are typically more similar between individuals with higher genetic relatedness (Engel et al, 2020; Selber‐Hnatiw et al, 2020). For instance, although human gut microbiomes can be highly variable, with each individual person having a unique microbiota (Rosenberg & Zilber‐Rosenberg, 2014), there is a higher microbiome similarity between related individuals such as identical twins (Goodrich et al, 2016; Selber‐Hnatiw et al, 2020) and similar trends have been observed for other species (Benson et al, 2010; Fietz et al, 2018; Griffiths et al, 2018; Pearce et al, 2017; Uren Webster et al, 2018).…”

Effects of short-term experimental manipulation of captive social environment on uropygial gland microbiome and preen oil volatile composition

“…This finding was upheld even when the nestlings were unrelated to one or both parents, either as the result of extra-pair fertilizations (dark-eyed juncos) or cross-fostering (Eurasian hoopoes). Similarly, members of the same zebra finch families had similar skin microbiomes, and spatial proximity of nest sites correlated with similarity between families (Engel et al, 2020). However, a study of Leach's storm petrels found that mated males and females were not more similar to each other at their uropygial and skin microbiomes than randomly selected individuals from the population (Pearce et al, 2017).…”

“…Social environment has been shown to play an important role in microbiome composition, as skin and gut bacterial communities reflect group membership and social networks in several mammalian (Song et al, 2013;Theis et al, 2013;Leclaire et al, 2014;Tung et al, 2015;Moeller et al, 2016;Yarlagadda et al, 2021) and avian (Kulkarni and Heeb, 2007;Ruiz-Rodríguez et al, 2014;Whittaker et al, 2016;Goodenough et al, 2017;Engel, et al, 2020) species. Indeed, behaviors that promote the transmission of beneficial microbes have been documented in several animal species, such as overmarking or allomarking in scent-marking animals (Buesching et al, 2003;Theis et al, 2008) and coprophagy (Osawa et al, 1993;Kobayashi et al, 2019), though microbe transmission can occur through other social behaviors like grooming and play (Meadow et al, 2013;Perofsky et al, 2017).…”